Skip to main content
Log in

Genetic Dissection of Component Traits for Salinity Tolerance at Reproductive Stage in Rice

  • Original Article
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Rice is highly sensitive to salt stress at flowering stage. With the objective of detection of quantitative trait loci (QTLs) in multi-environment for this stage, 180 backcross-derived lines (BC3F5) from salt tolerant donor Pokkali (AC41585) and recurrent parent IR 64 were subjected to evaluation in saline (EC = 8 dSm−1) and non-saline environments in wet season of 2014 and 2015 employing a novel phenotyping protocol. Nine multi-environmental consistent QTLs for spikelet degeneration, K+ concentration in flag leaf, stress susceptibility index for grain (SSI-Grain) and spikelet sterility (SSI-STE) on chromosomes1, 2, 3, 4 and 11 with 17–42% phenotypic variances were detected. Among several digenic epistatic interactions, one was associated with the main effect QTL (qSSI-STE-11-1) over the years. Similarly genotype × environment interaction associated with two additive QTLs, qDEG-S-2-2 and qSSI-STE-2-1 had positive effect on the resultant phenotype. Functional genes encoding calmodulin-binding protein and potassium transporter were predicted inside the consistent QTLs. Detected stable QTLs, associated markers, predicted genes and derived introgression lines with these QTLs could be utilized in future breeding programme.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abdullah Z, Khan A, Mushtaq, Flowers TJ (2001) Causes of sterility in seed set of rice under salinity stress. J Agron Crop Sci 187:25–32. https://doi.org/10.1046/j.1439-037X.2001.00500.x

    Article  Google Scholar 

  • Ammar MHM, Pandit A, Singh RK, Sameena S, Chauhan MS, Singh AK, Sharma PC, Gaikwad K, Sharma TR, Mohapatra T, Singh NK (2009) Mapping of QTLs controlling Na+, K+ and Cl- ion concentrations in salt tolerant indica rice variety CSR27. J Plant Biochem Biotechnol 18:139–150

    Article  CAS  Google Scholar 

  • Bonilla P, Dvorak J, Mackill D, Deal K, Gregorio G (2002) RFLP and SSLP mapping of salinity tolerance genes in chromosome 1 of rice (Oryza sativa L.) using recombinant inbred lines. Philip J Agric Sci 85:68–76

    Google Scholar 

  • Bouslama M, Schapaugh WT (1984) Stress tolerance in soybean. Part. 1: evaluation of three screening techniques for heat and drought tolerance. Crop Sci 24:933–937

    Article  Google Scholar 

  • Chakraborty K, Bose J, Shabala L, Shabala S (2016) Difference in root K+ retention ability and reduced sensitivity of K+-permeable channels to reactive oxygen species confer differential salt tolerance in three Brassica species. J Exp Bot 67(15):4611–4625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chakraborty K, Basak N, Bhaduri D, Ray S, Vijayan J, Chattopadhyay K, Sarkar RK (2018) Ionic basis of salt tolerance in plants: nutrient homeostasis and oxidative stress tolerance. In Hasanuzzaman M, Fujita M, Oku H, Nahar K, Hawrylak-Nowak B (eds.) Plant nutrients and abiotic stress tolerance. Springer, Singapore, pp 325– 362. https://doi.org/10.1007/978-981-10-9044-8_14

  • Chakraborty K, Chattaopadhyay K, Nayak L, Ray S, Yeasmin L, Jena P, Gupta S, Mohanty SK, Swain P, Sarkar RK (2019) Ionic selectivity and coordinated transport of Na+ and K+ in flag leaves render differential salt tolerance in rice at the reproductive stage. Planta 250:1637–1653. https://doi.org/10.1007/s00425-019-03253-9

    Article  CAS  PubMed  Google Scholar 

  • Chattopadhyay K, Nath D, Das G, Mohanta RL, Marndi BC, Singh DP, Sarkar RK, Singh ON (2013) Phenotyping and QTL-linked marker-based genotyping of rice lines with varying level of salt tolerance at flowering stage. Indian J Genet 73(4):434–437

    Google Scholar 

  • Chattopadhyay K, Marndi BC, Sarkar RK, Singh ON (2017) Stability analysis of backcross population for salinity tolerance at reproductive stage in rice. Indian J Genet 77(1):51–58. https://doi.org/10.5958/0975-6906.2017.00007.4

    Article  Google Scholar 

  • Chattopadhyay K, Nayak AK, Marndi BC, Poonam A, Chakraborty K, Sarkar RK (2018) Novel screening protocol for precise phenotyping of salt-tolerance at reproductive stage in rice. Physiol Mol Biol Plants 24(6):1047–1058. https://doi.org/10.1007/s12298-018-0591-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen G, Hu Q, Luo LE, Yang T, Zhang S, Hu Y, Yu L, Xu G (2015) Rice potassium transporter OsHAK1 is essential for maintaining potassium mediated growth and functions in salt tolerance over low and high potassium concentration ranges. Plant Cell Environ 38:2747–2765. https://doi.org/10.1111/pce.12585

    Article  CAS  PubMed  Google Scholar 

  • Chen G, Liu C, Gao Z, Zhang Y, Jiang H, Zhu L, Ren D, Yu L, Xu G, Qian Q (2017) OsHAK1, a high-affinity potassium transporter, positively regulates responses to drought stress in rice. Front Plant Sci 8:1885. https://doi.org/10.3389/fpls.2017.01885

    Article  PubMed  PubMed Central  Google Scholar 

  • Chinpongpanich A, Limruengroj K, Phean-o-pas S, Limpaseni T, Buaboocha T (2012) Expression analysis of calmodulin and calmodulin-like genes from rice, Oryzasativa L. BMC Res Notes 5:625–625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Demidchik V, Tester M (2002) Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol 128:379–387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620

    Article  CAS  PubMed  Google Scholar 

  • Eleuch L, Jilal A, Grando S, Ceccarelli S, Schmising MVK, Tsujimoto H, Hajer A, Daaloul A, Baum M (2008) Genetic diversity and association analysis for salinity tolerance, heading date and plant height of barley germplasm using simple sequence repeat markers. J Integr Plant Biol 50:1004–1014

    Article  CAS  PubMed  Google Scholar 

  • Federer WT, Wolfinger RD (1996) Gauss and SAS for recovering inter block and inter variety information. Technical Report Series of the Biometrics Unit, Cornell University, Ithaca

  • Fischer RA, Maurer R (1978) Drought resistance in spring wheat cultivars. I. Grain yield response. Aus J Agric Res 29:897–907

    Article  Google Scholar 

  • Ganie SA, Molla KA, Henry RJ, Bhat KV, Mondal TK (2019) Advances in understanding salt tolerance in rice. Theo Appl Genet 132(4):851–870

    Article  CAS  Google Scholar 

  • Gregorio G B, Senadhira D, Mendoza R D (1997) Screening rice for salinity tolerance. IRRI discussion paper series no. 22. Manila (Philippines), International Rice Research Institute, pp. 1-30

  • Hossain H, Rahman MA, Alam MS, Singh RK (2015) Mapping of quantitative trait loci associated with reproductive-stage salt tolerance in Rice. J Agron Crop Sci 201:17–31

    Article  CAS  Google Scholar 

  • Islam MR, Gregorio GB, Salam MA, Collard BCY, Singh RK, Hassan L (2012) Validation of SalTollinked markers and haplotype diversity on chromosome 1 of rice. Mol Plant Breed 3(10):103–114

    Google Scholar 

  • Kawahara Y et al (2013) Improvement of the OryzasativaNipponbare reference genome using next generation sequence and optical map data. Rice 6(1):4

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar A, Dixit S, Ram T, Yadav RB, Mishra KK, Mandal NP (2014) Breeding high-yielding drought-tolerant rice: genetic variations and conventional and molecular approaches. J Exp Bot 65(21):6265–6278. https://doi.org/10.1093/jxb/eru363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar V, Singh A, Amitha Mithra SV, Krishnamurthy SL, Parida SK, Jain S, Tiwari KK, Kumar P, Rao AR, Sharma SK, Khurana JP, Singh NK, Mohapatra T (2015) Genome-wide association mapping of salinity tolerance in rice (Oryza sativa). DNA Res 22:1–13. https://doi.org/10.1093/dnares/dsu046

    Article  CAS  Google Scholar 

  • Kurata N, Yamazaki Y (2006) Oryza base: an integrated biological and genome information database for rice. Plant Physiol 140(1):12–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Fan Y, Mak M, Babla M, Holford P, Wang F, Chen G, Scott G, Wang G, Shabala S, Zhou M, Chen Z-H (2017) QTLs for stomatal and photosynthetic traits related to salinity tolerance in barley. BMC Genomics 18:9. https://doi.org/10.1186/s12864-016-3380-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez-Atienza J, Jiang X, Garciablades B, Mendoza I, Zhu JK, Pardo JM, Quintero FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001–1012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng L, Li H, Zhang L, Wang J (2015) QTL Ici mapping: integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. Crop J 3:269–283

    Article  Google Scholar 

  • Molla KA, Debnath AB, Ganie SA, Mondal TK (2015) Identification and analysis of novel salt responsive candidate gene based SSRs (cgSSRs) from rice (Oryza sativa L.). BMC Plant Biol 15(1):1

    Article  CAS  Google Scholar 

  • Moradi F, Ismail AM (2007) Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Ann Bot 99:1161–1173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Bio 59:651–681

    Article  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325. https://doi.org/10.1093/nar/8.19.4321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pandit A, Rai V, Bal S, Sinha S, Kumar V, Chauhan M, Gautam RK, Singh R, Sharma PC, Singh AK, Gaikwad K, Sharma TR, Mohapatra T, Singh NK (2010) Combining QTL mapping and transcriptome profiling of bulked RILs for identification of functional polymorphism for salt tolerance genes in rice (Oryza sativa L.). Mol Genet Genomics 284:121–136. https://doi.org/10.1007/s00438-010-0551-6

    Article  CAS  PubMed  Google Scholar 

  • Rahman MA, Bimpong IK, Bizimana JB, Pascual ED, Arceta M, Swamy MAM, Diaw F, Rahman MS, Singh RK (2017) Mapping QTLs using a novel source of salinity tolerance from Hasawi and their interaction with environments in rice. Rice 10:47. https://doi.org/10.1186/s12284-017-0186-x

    Article  PubMed  PubMed Central  Google Scholar 

  • Razzaque S, Haque T, Elias SM, RahmanMd S, Biswas S, Schwartz S, Ismail AM, Walia H, Juenger TE, Seraj ZI (2017) Reproductive stage physiological and transcriptional responses to salinity stress in reciprocal populations derived from tolerant (Horkuch) and susceptible (IR29) Rice. Sci Rep 7:46138. https://doi.org/10.1038/srep46138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reza M, Mendioro MS, Diaz GQ, Gregorio GB, Singh RK (2013) Mapping quantitative trait loci associated with yield and yield components under reproductive stage salinity stress in rice (OryzaSativa). J Genet 92:433–443

    Article  Google Scholar 

  • Saha A, Sarkar RK, Yamagishi Y (1998) Effect of time of nitrogen application on spikelet differentiation and degeneration of rice. Bot Bull Acad Sin 39:119–123

    Google Scholar 

  • Sakai H, Lee SS, Tanaka T, Numa H, Kim J, Kawahara Y, Wakimoto H, Yang CC, Iwamoto M, Abe T, Yamada Y, Muto A, Inokuchi H, Ikemura T, Matsumoto T, Sasaki T, Itoh T (2013) Rice Annotation Project Database (RAP-DB): an integrative and interactive database for rice genomics. Plant Cell Physiol 54(2):e6–e6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt R, Mieulet D, Hubberten HM, Obata T, Hoefgen R, Fernie AR, Fisahn J, Segundo BS, Guiderdoni E, Schippers JHM, Mueller-Roeber B (2013) Salt-responsive ERF1 regulates reactive oxygen species-dependent signaling during the initial response to salt stress in rice. Plant Cell 25(6):2115–2131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141:1653–1665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh H, Deshmukh RK, Singh A, Singh AK, Gaikwad K, Sharma TR, Mohapatra T, Singh NK (2009) Highly variable SSR markers suitable for rice genotyping using agarose gels. Mol Breed 25:359–364

    Article  Google Scholar 

  • Surekha R, Mishra PB, Gupta SR, Rathore A (2008) Reproductive stage tolerance to salinity and alkalinity stresses in rice genotypes. Plant Breed 127:256–261

    Article  Google Scholar 

  • Tiwari S, Krishnamurthy SL, Kumar V, Singh B, Rao A, Mithra SV, Rai V, Singh AK, Singh NK (2016) Mapping QTLs for salt tolerance in Rice (Oryzasativa L.) by bulked segregant analysis of recombinant inbred lines using 50K SNP chip. PLoS ONE 11(4):e0153610. https://doi.org/10.1371/journal.pone.0153610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Berloo R (2008) GGT 2.0: versatile software for visualization and analysis of genetic data. J Hered 99:232–236

    Article  PubMed  Google Scholar 

  • Wolfinger RD, Federer WT, Cordero-Brana O (1997) Recovering information in augmented designs, using SAS PROC GLM and PROC MIXED. Agron J 89:856–859

    Article  Google Scholar 

  • Xue D, Huang Y, Zhang X, Wei K, Westcott S, Li C, Chen M, Zhang G, Lance R (2009) Identification of QTLs associated with salinity tolerance at late growth stage in barley. Euphytica 169:187–196

    Article  Google Scholar 

  • Yamamoto E, Yonemaru JI, Yamamoto T, Yano M (2012) OGRO: the overview of functionally characterized genes in rice online database. Rice 5(1):26

    Article  PubMed  PubMed Central  Google Scholar 

  • Yokoyama C, Tsuda M, Hirai Y (2002) Effects of plant growth regulators on number of spikelets per panicle in Rice (Oryzasativa L.) under saline flooding conditions. Crop Physiol Cell Biol 71(3):376–382

    CAS  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice, 3rd edn. IRRI, Los Banos, pp 61–66

    Google Scholar 

  • Zeng L, Shannon MC (2000) Salinity effects on the seedling growth and yield components of rice. Crop Sci 40:996–1003

    Article  Google Scholar 

  • Zeng L, Shannon MC, Grieve CM (2002) Evaluation of salt tolerance in rice genotypes by multiple agronomic parameters. Euphytica 127:235–245

    Article  CAS  Google Scholar 

Download references

Funding

Authors acknowledge received funding from the Director, ICAR-National Rice Research Institute, Cuttack and ICAR funded project ‘National Innovation on Climate Resilient Agriculture’, New Delhi.

Author information

Authors and Affiliations

Authors

Contributions

KC made design of the experiment and drafted manuscript. SKM, JV and BCM implemented experiments and analyse data. RKS coordinated the study. KAM and JV assisted in selection of markers and linkage mapping. AS statistically analysed the data. SR analysed molecular data. KOC and RKS assisted in preparing manuscript and revised the manuscript.

Corresponding author

Correspondence to Krishnendu Chattopadhyay.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Key message

• Employing a population using salt tolerant donor at reproductive stage, Pokkali (AC 41585), nine multi-environmental consistent QTLs for spikelet degeneration, spikelet sterility, K+ concentration at flag leaf, etc. were discovered.

• Two genotype × environment interaction QTLs and one digenic-epistatic QTL were detected with synergistic effect on the main effect QTLs.

Supplementary Information

ESM 1

(DOC 1414 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chattopadhyay, K., Mohanty, S.K., Vijayan, J. et al. Genetic Dissection of Component Traits for Salinity Tolerance at Reproductive Stage in Rice. Plant Mol Biol Rep 39, 386–402 (2021). https://doi.org/10.1007/s11105-020-01257-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-020-01257-4

Keywords

Navigation